Gluconeogenesis and PEPCK are critical components of healthy aging and dietary restriction life extension


Autoři: Brian Onken aff001;  Natallia Kalinava aff001;  Monica Driscoll aff001
Působiště autorů: Department of Molecular Biology and Biochemistry Rutgers University, Piscataway, NJ, United States of America aff001
Vyšlo v časopise: Gluconeogenesis and PEPCK are critical components of healthy aging and dietary restriction life extension. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008982
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008982

Souhrn

High glucose diets are unhealthy, although the mechanisms by which elevated glucose is harmful to whole animal physiology are not well understood. In Caenorhabditis elegans, high glucose shortens lifespan, while chemically inflicted glucose restriction promotes longevity. We investigated the impact of glucose metabolism on aging quality (maintained locomotory capacity and median lifespan) and found that, in addition to shortening lifespan, excess glucose negatively impacts locomotory healthspan. Conversely, disrupting glucose utilization by knockdown of glycolysis-specific genes results in large mid-age physical improvements via a mechanism that requires the FOXO transcription factor DAF-16. Adult locomotory capacity is extended by glycolysis disruption, but maximum lifespan is not, indicating that limiting glycolysis can increase the proportion of life spent in mobility health. We also considered the largely ignored role of glucose biosynthesis (gluconeogenesis) in adult health. Directed perturbations of gluconeogenic genes that specify single direction enzymatic reactions for glucose synthesis decrease locomotory healthspan, suggesting that gluconeogenesis is needed for healthy aging. Consistent with this idea, overexpression of the central gluconeogenic gene pck-2 (encoding PEPCK) increases health measures via a mechanism that requires DAF-16 to promote pck-2 expression in specific intestinal cells. Dietary restriction also features DAF-16-dependent pck-2 expression in the intestine, and the healthspan benefits conferred by dietary restriction require pck-2. Together, our results describe a new paradigm in which nutritional signals engage gluconeogenesis to influence aging quality via DAF-16. These data underscore the idea that promotion of gluconeogenesis might be an unappreciated goal for healthy aging and could constitute a novel target for pharmacological interventions that counter high glucose consequences, including diabetes.

Klíčová slova:

Biological locomotion – Caenorhabditis elegans – Gastrointestinal tract – Gene disruption – Glucose – Glucose metabolism – Glycolysis – RNA interference


Zdroje

1. de Cabo R, Carmona-Gutierrez D, Bernier M, Hall MN, Madeo F. The search for antiaging interventions: from elixirs to fasting regimens. Cell. 2014;157(7):1515–26. Epub 2014/06/21. doi: 10.1016/j.cell.2014.05.031 24949965; PubMed Central PMCID: PMC4254402.

2. Adler AI, Boyko EJ, Ahroni JH, Stensel V, Forsberg RC, Smith DG. Risk factors for diabetic peripheral sensory neuropathy. Results of the Seattle Prospective Diabetic Foot Study. Diabetes care. 1997;20(7):1162–7. Epub 1997/07/01. doi: 10.2337/diacare.20.7.1162 9203456.

3. Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA: the journal of the American Medical Association. 2002;287(3):356–9. Epub 2002/01/16. doi: 10.1001/jama.287.3.356 11790215.

4. Hanefeld M, Fischer S, Julius U, Schulze J, Schwanebeck U, Schmechel H, et al. Risk factors for myocardial infarction and death in newly detected NIDDM: the Diabetes Intervention Study, 11-year follow-up. Diabetologia. 1996;39(12):1577–83. Epub 1996/12/01. doi: 10.1007/s001250050617 8960845.

5. Klein R. Hyperglycemia and microvascular and macrovascular disease in diabetes. Diabetes care. 1995;18(2):258–68. Epub 1995/02/01. doi: 10.2337/diacare.18.2.258 7729308.

6. Standl E, Balletshofer B, Dahl B, Weichenhain B, Stiegler H, Hormann A, et al. Predictors of 10-year macrovascular and overall mortality in patients with NIDDM: the Munich General Practitioner Project. Diabetologia. 1996;39(12):1540–5. Epub 1996/12/01. doi: 10.1007/s001250050612 8960840.

7. Uusitupa MI, Niskanen LK, Siitonen O, Voutilainen E, Pyorala K. Ten-year cardiovascular mortality in relation to risk factors and abnormalities in lipoprotein composition in type 2 (non-insulin-dependent) diabetic and non-diabetic subjects. Diabetologia. 1993;36(11):1175–84. Epub 1993/11/01. doi: 10.1007/BF00401063 8270133.

8. Wei M, Gaskill SP, Haffner SM, Stern MP. Effects of diabetes and level of glycemia on all-cause and cardiovascular mortality. The San Antonio Heart Study. Diabetes care. 1998;21(7):1167–72. Epub 1998/07/08. doi: 10.2337/diacare.21.7.1167 9653614.

9. American Diabetes A, Bantle JP, Wylie-Rosett J, Albright AL, Apovian CM, Clark NG, et al. Nutrition recommendations and interventions for diabetes: a position statement of the American Diabetes Association. Diabetes care. 2008;31 Suppl 1:S61–78. Epub 2008/01/10. doi: 10.2337/dc08-S061 18165339.

10. Ostler JE, Maurya SK, Dials J, Roof SR, Devor ST, Ziolo MT, et al. Effects of insulin resistance on skeletal muscle growth and exercise capacity in type 2 diabetic mouse models. Am J Physiol Endocrinol Metab. 2014;306(6):E592–605. Epub 2014/01/16. doi: 10.1152/ajpendo.00277.2013 24425761; PubMed Central PMCID: PMC3948983.

11. Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes care. 2009;32(11):1993–7. Epub 2009/06/25. doi: 10.2337/dc09-0264 19549734; PubMed Central PMCID: PMC2768193.

12. Park SW, Goodpaster BH, Strotmeyer ES, Kuller LH, Broudeau R, Kammerer C, et al. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes care. 2007;30(6):1507–12. Epub 2007/03/17. doi: 10.2337/dc06-2537 17363749.

13. Alcantar-Fernandez J, Navarro RE, Salazar-Martinez AM, Perez-Andrade ME, Miranda-Rios J. Caenorhabditis elegans respond to high-glucose diets through a network of stress-responsive transcription factors. PLoS One. 2018;13(7):e0199888. Epub 2018/07/11. doi: 10.1371/journal.pone.0199888 29990370; PubMed Central PMCID: PMC6039004.

14. Choi SS. High glucose diets shorten lifespan of Caenorhabditis elegans via ectopic apoptosis induction. Nutr Res Pract. 2011;5(3):214–8. Epub 2011/07/23. doi: 10.4162/nrp.2011.5.3.214 21779524; PubMed Central PMCID: PMC3133753.

15. Dobson AJ, Ezcurra M, Flanagan CE, Summerfield AC, Piper MDW, Gems D, et al. Nutritional Programming of Lifespan by FOXO Inhibition on Sugar-Rich Diets. Cell Rep. 2017;18(2):299–306. Epub 2017/01/12. doi: 10.1016/j.celrep.2016.12.029 28076775; PubMed Central PMCID: PMC5263231.

16. Lee SJ, Murphy CT, Kenyon C. Glucose shortens the life span of C. elegans by downregulating DAF-16/FOXO activity and aquaporin gene expression. Cell Metab. 2009;10(5):379–91. Epub 2009/11/04. doi: 10.1016/j.cmet.2009.10.003 19883616; PubMed Central PMCID: PMC2887095.

17. Marcellino BK, Ekasumara N, Mobbs CV. Dietary Restriction and Glycolytic Inhibition Reduce Proteotoxicity and Extend Lifespan via NHR-49. Curr Neurobiol. 2018;9(1):1–7. Epub 2019/03/02. 30820135; PubMed Central PMCID: PMC6390974.

18. Schlotterer A, Kukudov G, Bozorgmehr F, Hutter H, Du X, Oikonomou D, et al. C. elegans as model for the study of high glucose- mediated life span reduction. Diabetes. 2009;58(11):2450–6. Epub 2009/08/14. doi: 10.2337/db09-0567 19675139; PubMed Central PMCID: PMC2768179.

19. Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 2007;6(4):280–93. Epub 2007/10/03. doi: 10.1016/j.cmet.2007.08.011 17908557.

20. Seo Y, Kingsley S, Walker G, Mondoux MA, Tissenbaum HA. Metabolic shift from glycogen to trehalose promotes lifespan and healthspan in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2018;115(12):E2791–E800. Epub 2018/03/08. doi: 10.1073/pnas.1714178115 29511104; PubMed Central PMCID: PMC5866546.

21. Friedman DB, Johnson TE. A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics. 1988;118(1):75–86. Epub 1988/01/01. 8608934; PubMed Central PMCID: PMC1203268.

22. Hsu AL, Murphy CT, Kenyon C. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science. 2003;300(5622):1142–5. Epub 2003/05/17. doi: 10.1126/science.1083701 12750521.

23. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature. 1993;366(6454):461–4. Epub 1993/12/02. doi: 10.1038/366461a0 8247153.

24. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science. 1997;277(5328):942–6. Epub 1997/08/15. doi: 10.1126/science.277.5328.942 9252323.

25. Lin K, Dorman JB, Rodan A, Kenyon C. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science. 1997;278(5341):1319–22. Epub 1997/11/21. doi: 10.1126/science.278.5341.1319 9360933.

26. Morris JZ, Tissenbaum HA, Ruvkun G. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature. 1996;382(6591):536–9. Epub 1996/08/08. doi: 10.1038/382536a0 8700226.

27. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY, Liu S, et al. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell. 2008;132(6):1025–38. Epub 2008/03/25. doi: 10.1016/j.cell.2008.01.030 18358814; PubMed Central PMCID: PMC2367249.

28. Vowels JJ, Thomas JH. Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics. 1992;130(1):105–23. Epub 1992/01/01. 1732156; PubMed Central PMCID: PMC1204785.

29. Priebe S, Menzel U, Zarse K, Groth M, Platzer M, Ristow M, et al. Extension of life span by impaired glucose metabolism in Caenorhabditis elegans is accompanied by structural rearrangements of the transcriptomic network. PLoS One. 2013;8(10):e77776. Epub 2013/11/10. doi: 10.1371/journal.pone.0077776 24204961; PubMed Central PMCID: PMC3813781.

30. Lee CK, Allison DB, Brand J, Weindruch R, Prolla TA. Transcriptional profiles associated with aging and middle age-onset caloric restriction in mouse hearts. Proc Natl Acad Sci U S A. 2002;99(23):14988–93. Epub 2002/11/07. doi: 10.1073/pnas.232308999 12419851; PubMed Central PMCID: PMC137532.

31. Masoro EJ, McCarter RJ, Katz MS, McMahan CA. Dietary restriction alters characteristics of glucose fuel use. J Gerontol. 1992;47(6):B202–8. Epub 1992/11/01. doi: 10.1093/geronj/47.6.b202 1430849.

32. Mobbs CV, Mastaitis JW, Zhang M, Isoda F, Cheng H, Yen K. Secrets of the lac operon. Glucose hysteresis as a mechanism in dietary restriction, aging and disease. Interdiscip Top Gerontol. 2007;35:39–68. Epub 2006/10/26. doi: 10.1159/000096555 17063032; PubMed Central PMCID: PMC2755292.

33. Bishop NA, Guarente L. Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature. 2007;447(7144):545–9. Epub 2007/06/01. doi: 10.1038/nature05904 17538612.

34. Greer EL, Brunet A. Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell. 2009;8(2):113–27. Epub 2009/02/26. doi: 10.1111/j.1474-9726.2009.00459.x 19239417; PubMed Central PMCID: PMC2680339.

35. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, et al. An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol. 2007;17(19):1646–56. Epub 2007/09/29. doi: 10.1016/j.cub.2007.08.047 17900900; PubMed Central PMCID: PMC2185793.

36. Houthoofd K, Braeckman BP, Johnson TE, Vanfleteren JR. Life extension via dietary restriction is independent of the Ins/IGF-1 signalling pathway in Caenorhabditis elegans. Exp Gerontol. 2003;38(9):947–54. Epub 2003/09/05. doi: 10.1016/s0531-5565(03)00161-x 12954481.

37. Kaeberlein TL, Smith ED, Tsuchiya M, Welton KL, Thomas JH, Fields S, et al. Lifespan extension in Caenorhabditis elegans by complete removal of food. Aging Cell. 2006;5(6):487–94. Epub 2006/11/04. doi: 10.1111/j.1474-9726.2006.00238.x 17081160.

38. Lakowski B, Hekimi S. The genetics of caloric restriction in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1998;95(22):13091–6. Epub 1998/10/28. doi: 10.1073/pnas.95.22.13091 9789046; PubMed Central PMCID: PMC23719.

39. Lee GD, Wilson MA, Zhu M, Wolkow CA, de Cabo R, Ingram DK, et al. Dietary deprivation extends lifespan in Caenorhabditis elegans. Aging Cell. 2006;5(6):515–24. Epub 2006/11/14. doi: 10.1111/j.1474-9726.2006.00241.x 17096674; PubMed Central PMCID: PMC2546582.

40. Masoro EJ. Overview of caloric restriction and ageing. Mech Ageing Dev. 2005;126(9):913–22. Epub 2005/05/12. doi: 10.1016/j.mad.2005.03.012 15885745.

41. Onken B, Driscoll M. Metformin induces a dietary restriction-like state and the oxidative stress response to extend C. elegans Healthspan via AMPK, LKB1, and SKN-1. PLoS One. 2010;5(1):e8758. Epub 2010/01/22. doi: 10.1371/journal.pone.0008758 20090912; PubMed Central PMCID: PMC2807458.

42. Panowski SH, Wolff S, Aguilaniu H, Durieux J, Dillin A. PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans. Nature. 2007;447(7144):550–5. Epub 2007/05/04. doi: 10.1038/nature05837 17476212.

43. Walker G, Houthoofd K, Vanfleteren JR, Gems D. Dietary restriction in C. elegans: from rate-of-living effects to nutrient sensing pathways. Mech Ageing Dev. 2005;126(9):929–37. Epub 2005/05/18. doi: 10.1016/j.mad.2005.03.014 15896824.

44. Glenn CF, Chow DK, David L, Cooke CA, Gami MS, Iser WB, et al. Behavioral deficits during early stages of aging in Caenorhabditis elegans result from locomotory deficits possibly linked to muscle frailty. The journals of gerontology Series A, Biological sciences and medical sciences. 2004;59(12):1251–60. Epub 2005/02/09. doi: 10.1093/gerona/59.12.1251 15699524; PubMed Central PMCID: PMC1458366.

45. Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, et al. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature. 2002;419(6909):808–14. Epub 2002/10/25. doi: 10.1038/nature01135 12397350.

46. Liu J, Zhang B, Lei H, Feng Z, Liu J, Hsu AL, et al. Functional aging in the nervous system contributes to age-dependent motor activity decline in C. elegans. Cell Metab. 2013;18(3):392–402. Epub 2013/09/10. doi: 10.1016/j.cmet.2013.08.007 24011074; PubMed Central PMCID: PMC3811915.

47. Toth ML, Melentijevic I, Shah L, Bhatia A, Lu K, Talwar A, et al. Neurite sprouting and synapse deterioration in the aging Caenorhabditis elegans nervous system. J Neurosci. 2012;32(26):8778–90. Epub 2012/06/30. doi: 10.1523/JNEUROSCI.1494-11.2012 22745480; PubMed Central PMCID: PMC3427745.

48. Chow DK, Glenn CF, Johnston JL, Goldberg IG, Wolkow CA. Sarcopenia in the Caenorhabditis elegans pharynx correlates with muscle contraction rate over lifespan. Exp Gerontol. 2006;41(3):252–60. Epub 2006/02/01. doi: 10.1016/j.exger.2005.12.004 16446070; PubMed Central PMCID: PMC2553216.

49. Evason K, Huang C, Yamben I, Covey DF, Kornfeld K. Anticonvulsant medications extend worm life-span. Science. 2005;307(5707):258–62. Epub 2005/01/18. doi: 10.1126/science.1105299 15653505.

50. Laranjeiro R, Harinath G, Burke D, Braeckman BP, Driscoll M. Single swim sessions in C. elegans induce key features of mammalian exercise. BMC biology. 2017;15(1):30. Epub 2017/04/12. doi: 10.1186/s12915-017-0368-4 28395669; PubMed Central PMCID: PMC5385602.

51. Laranjeiro R, Harinath G, Hewitt JE, Hartman JH, Royal MA, Meyer JN, et al. Swim exercise in Caenorhabditis elegans extends neuromuscular and gut healthspan, enhances learning ability, and protects against neurodegeneration. Proc Natl Acad Sci U S A. 2019;116(47):23829–39. Epub 2019/11/07. doi: 10.1073/pnas.1909210116 31685639; PubMed Central PMCID: PMC6876156.

52. Lee D, Jeong DE, Son HG, Yamaoka Y, Kim H, Seo K, et al. SREBP and MDT-15 protect C. elegans from glucose-induced accelerated aging by preventing accumulation of saturated fat. Genes Dev. 2015;29(23):2490–503. Epub 2015/12/08. doi: 10.1101/gad.266304.115 26637528; PubMed Central PMCID: PMC4691952.

53. Hayward RA, Reaven PD, Emanuele NV, Investigators V. Follow-up of Glycemic Control and Cardiovascular Outcomes in Type 2 Diabetes. The New England journal of medicine. 2015;373(10):978. Epub 2015/09/04. doi: 10.1056/NEJMc1508386 26332555.

54. Bansal A, Zhu LJ, Yen K, Tissenbaum HA. Uncoupling lifespan and healthspan in Caenorhabditis elegans longevity mutants. Proc Natl Acad Sci U S A. 2015;112(3):E277–86. Epub 2015/01/07. doi: 10.1073/pnas.1412192112 25561524; PubMed Central PMCID: PMC4311797.

55. Furuyama T, Nakazawa T, Nakano I, Mori N. Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem J. 2000;349(Pt 2):629–34. Epub 2000/07/06. doi: 10.1042/0264-6021:3490629 10880363; PubMed Central PMCID: PMC1221187.

56. Honda Y, Honda S. The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 1999;13(11):1385–93. Epub 1999/07/31. 10428762.

57. Yang J, Kalhan SC, Hanson RW. What is the metabolic role of phosphoenolpyruvate carboxykinase? J Biol Chem. 2009;284(40):27025–9. Epub 2009/07/29. doi: 10.1074/jbc.R109.040543 19636077; PubMed Central PMCID: PMC2785631.

58. Hakimi P, Yang J, Casadesus G, Massillon D, Tolentino-Silva F, Nye CK, et al. Overexpression of the cytosolic form of phosphoenolpyruvate carboxykinase (GTP) in skeletal muscle repatterns energy metabolism in the mouse. J Biol Chem. 2007;282(45):32844–55. Epub 2007/08/25. doi: 10.1074/jbc.M706127200 17716967; PubMed Central PMCID: PMC4484620.

59. Yuan Y, Kadiyala CS, Ching TT, Hakimi P, Saha S, Xu H, et al. Enhanced energy metabolism contributes to the extended life span of calorie-restricted Caenorhabditis elegans. J Biol Chem. 2012;287(37):31414–26. Epub 2012/07/20. doi: 10.1074/jbc.M112.377275 22810224; PubMed Central PMCID: PMC3438970.

60. van Schaftingen E, Gerin I. The glucose-6-phosphatase system. Biochem J. 2002;362(Pt 3):513–32. Epub 2002/03/07. doi: 10.1042/0264-6021:3620513 11879177; PubMed Central PMCID: PMC1222414.

61. Wang J, Kim SK. Global analysis of dauer gene expression in Caenorhabditis elegans. Development. 2003;130(8):1621–34. Epub 2003/03/07. doi: 10.1242/dev.00363 12620986.

62. Halaschek-Wiener J, Khattra JS, McKay S, Pouzyrev A, Stott JM, Yang GS, et al. Analysis of long-lived C. elegans daf-2 mutants using serial analysis of gene expression. Genome research. 2005;15(5):603–15. Epub 2005/04/20. doi: 10.1101/gr.3274805 15837805; PubMed Central PMCID: PMC1088289.

63. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, et al. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature. 2003;424(6946):277–83. Epub 2003/07/08. doi: 10.1038/nature01789 12845331.

64. Gerstbrein B, Stamatas G, Kollias N, Driscoll M. In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans. Aging Cell. 2005;4(3):127–37. Epub 2005/06/01. doi: 10.1111/j.1474-9726.2005.00153.x 15924569.

65. Zhang M, Poplawski M, Yen K, Cheng H, Bloss E, Zhu X, et al. Role of CBP and SATB-1 in aging, dietary restriction, and insulin-like signaling. PLoS Biol. 2009;7(11):e1000245. Epub 2009/11/20. doi: 10.1371/journal.pbio.1000245 19924292; PubMed Central PMCID: PMC2774267.

66. Akasaki Y, Ouchi N, Izumiya Y, Bernardo BL, Lebrasseur NK, Walsh K. Glycolytic fast-twitch muscle fiber restoration counters adverse age-related changes in body composition and metabolism. Aging Cell. 2014;13(1):80–91. Epub 2013/09/17. doi: 10.1111/acel.12153 24033924; PubMed Central PMCID: PMC3947044.

67. Liggett MR, Hoy MJ, Mastroianni M, Mondoux MA. High-glucose diets have sex-specific effects on aging in C. elegans: toxic to hermaphrodites but beneficial to males. Aging (Albany NY). 2015;7(6):383–8. Epub 2015/07/06. doi: 10.18632/aging.100759 26143626; PubMed Central PMCID: PMC4505165.

68. Pappachan JM, Varughese GI, Sriraman R, Arunagirinathan G. Diabetic cardiomyopathy: Pathophysiology, diagnostic evaluation and management. World J Diabetes. 2013;4(5):177–89. Epub 2013/10/23. doi: 10.4239/wjd.v4.i5.177 24147202; PubMed Central PMCID: PMC3797883.

69. Cetrone M, Mele A, Tricarico D. Effects of the antidiabetic drugs on the age-related atrophy and sarcopenia associated with diabetes type II. Curr Diabetes Rev. 2014;10(4):231–7. Epub 2014/09/24. doi: 10.2174/1573399810666140918121022 25245021.

70. Schuster E, McElwee JJ, Tullet JM, Doonan R, Matthijssens F, Reece-Hoyes JS, et al. DamID in C. elegans reveals longevity-associated targets of DAF-16/FoxO. Mol Syst Biol. 2010;6:399. Epub 2010/08/14. doi: 10.1038/msb.2010.54 20706209; PubMed Central PMCID: PMC2950082.

71. Oh KJ, Han HS, Kim MJ, Koo SH. CREB and FoxO1: two transcription factors for the regulation of hepatic gluconeogenesis. BMB Rep. 2013;46(12):567–74. Epub 2013/11/19. doi: 10.5483/bmbrep.2013.46.12.248 24238363; PubMed Central PMCID: PMC4133859.

72. Salih DA, Brunet A. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol. 2008;20(2):126–36. Epub 2008/04/09. doi: 10.1016/j.ceb.2008.02.005 18394876; PubMed Central PMCID: PMC2387118.

73. Yuan Y, Hakimi P, Kao C, Kao A, Liu R, Janocha A, et al. Reciprocal Changes in Phosphoenolpyruvate Carboxykinase and Pyruvate Kinase with Age Are a Determinant of Aging in Caenorhabditis elegans. J Biol Chem. 2016;291(3):1307–19. Epub 2015/12/04. doi: 10.1074/jbc.M115.691766 26631730; PubMed Central PMCID: PMC4714217.

74. Libina N, Berman JR, Kenyon C. Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell. 2003;115(4):489–502. Epub 2003/11/19. doi: 10.1016/s0092-8674(03)00889-4 14622602.

75. Murphy CT, Lee SJ, Kenyon C. Tissue entrainment by feedback regulation of insulin gene expression in the endoderm of Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2007;104(48):19046–50. Epub 2007/11/21. doi: 10.1073/pnas.0709613104 18025456; PubMed Central PMCID: PMC2141905.

76. Giannakou ME, Goss M, Junger MA, Hafen E, Leevers SJ, Partridge L. Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science. 2004;305(5682):361. Epub 2004/06/12. doi: 10.1126/science.1098219 15192154.

77. Hwangbo DS, Gershman B, Tu MP, Palmer M, Tatar M. Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature. 2004;429(6991):562–6. Epub 2004/06/04. doi: 10.1038/nature02549 15175753.

78. Giannakou ME, Goss M, Jacobson J, Vinti G, Leevers SJ, Partridge L. Dynamics of the action of dFOXO on adult mortality in Drosophila. Aging Cell. 2007;6(4):429–38. Epub 2007/05/01. doi: 10.1111/j.1474-9726.2007.00290.x 17465980.

79. Webb AE, Kundaje A, Brunet A. Characterization of the direct targets of FOXO transcription factors throughout evolution. Aging Cell. 2016;15(4):673–85. Epub 2016/04/12. doi: 10.1111/acel.12479 27061590; PubMed Central PMCID: PMC4933671.

80. Vora M, Shah M, Ostafi S, Onken B, Xue J, Ni JZ, et al. Deletion of microRNA-80 activates dietary restriction to extend C. elegans healthspan and lifespan. PLoS Genet. 2013;9(8):e1003737. Epub 2013/09/07. doi: 10.1371/journal.pgen.1003737 24009527; PubMed Central PMCID: PMC3757059.

81. Hibshman JD, Doan AE, Moore BT, Kaplan RE, Hung A, Webster AK, et al. daf-16/FoxO promotes gluconeogenesis and trehalose synthesis during starvation to support survival. Elife. 2017;6. Epub 2017/10/25. doi: 10.7554/eLife.30057 29063832; PubMed Central PMCID: PMC5655125.

82. Gusarov I, Pani B, Gautier L, Smolentseva O, Eremina S, Shamovsky I, et al. Glycogen controls Caenorhabditis elegans lifespan and resistance to oxidative stress. Nature communications. 2017;8:15868. Epub 2017/06/20. doi: 10.1038/ncomms15868 28627510; PubMed Central PMCID: PMC5481799.

83. Fuchs S, Bundy JG, Davies SK, Viney JM, Swire JS, Leroi AM. A metabolic signature of long life in Caenorhabditis elegans. BMC biology. 2010;8:14. Epub 2010/02/12. doi: 10.1186/1741-7007-8-14 20146810; PubMed Central PMCID: PMC2829508.

84. McElwee JJ, Schuster E, Blanc E, Thornton J, Gems D. Diapause-associated metabolic traits reiterated in long-lived daf-2 mutants in the nematode Caenorhabditis elegans. Mech Ageing Dev. 2006;127(5):458–72. Epub 2006/03/09. doi: 10.1016/j.mad.2006.01.006 16522328.

85. Bujak AL, Crane JD, Lally JS, Ford RJ, Kang SJ, Rebalka IA, et al. AMPK activation of muscle autophagy prevents fasting-induced hypoglycemia and myopathy during aging. Cell Metab. 2015;21(6):883–90. Epub 2015/06/04. doi: 10.1016/j.cmet.2015.05.016 26039451; PubMed Central PMCID: PMC5233441.

86. Hansen M, Chandra A, Mitic LL, Onken B, Driscoll M, Kenyon C. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 2008;4(2):e24. Epub 2008/02/20. doi: 10.1371/journal.pgen.0040024 18282106; PubMed Central PMCID: PMC2242811.

87. Orlandi I, Stamerra G, Vai M. Altered Expression of Mitochondrial NAD(+) Carriers Influences Yeast Chronological Lifespan by Modulating Cytosolic and Mitochondrial Metabolism. Front Genet. 2018;9:676. Epub 2019/01/09. doi: 10.3389/fgene.2018.00676 30619489; PubMed Central PMCID: PMC6305841.

88. Post S, Karashchuk G, Wade JD, Sajid W, De Meyts P, Tatar M. Drosophila Insulin-Like Peptides DILP2 and DILP5 Differentially Stimulate Cell Signaling and Glycogen Phosphorylase to Regulate Longevity. Front Endocrinol (Lausanne). 2018;9:245. Epub 2018/06/13. doi: 10.3389/fendo.2018.00245 29892262; PubMed Central PMCID: PMC5985746.

89. Vall-Llaura N, Mir N, Garrido L, Vived C, Cabiscol E. Redox control of yeast Sir2 activity is involved in acetic acid resistance and longevity. Redox Biol. 2019;24:101229. Epub 2019/06/04. doi: 10.1016/j.redox.2019.101229 31153040; PubMed Central PMCID: PMC6543126.

90. Budovskaya YV, Wu K, Southworth LK, Jiang M, Tedesco P, Johnson TE, et al. An elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans. Cell. 2008;134(2):291–303. Epub 2008/07/30. doi: 10.1016/j.cell.2008.05.044 18662544; PubMed Central PMCID: PMC4719053.

91. Kashyap L, Perera S, Fisher AL. Identification of novel genes involved in sarcopenia through RNAi screening in Caenorhabditis elegans. The journals of gerontology Series A, Biological sciences and medical sciences. 2012;67(1):56–65. Epub 2011/05/20. doi: 10.1093/gerona/glr072 21593014; PubMed Central PMCID: PMC3260486.

92. Restif C, Ibanez-Ventoso C, Vora MM, Guo S, Metaxas D, Driscoll M. CeleST: computer vision software for quantitative analysis of C. elegans swim behavior reveals novel features of locomotion. PLoS Comput Biol. 2014;10(7):e1003702. Epub 2014/07/18. doi: 10.1371/journal.pcbi.1003702 25033081; PubMed Central PMCID: PMC4102393.

93. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77(1):71–94. Epub 1974/05/01. 4366476; PubMed Central PMCID: PMC1213120.

94. Kamath RS, Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods. 2003;30(4):313–21. Epub 2003/06/28. doi: 10.1016/s1046-2023(03)00050-1 12828945.

95. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature. 2003;421(6920):231–7. Epub 2003/01/17. doi: 10.1038/nature01278 12529635.

96. Pinan-Lucarre B, Gabel CV, Reina CP, Hulme SE, Shevkoplyas SS, Slone RD, et al. The core apoptotic executioner proteins CED-3 and CED-4 promote initiation of neuronal regeneration in Caenorhabditis elegans. PLoS Biol. 2012;10(5):e1001331. Epub 2012/05/26. doi: 10.1371/journal.pbio.1001331 22629231; PubMed Central PMCID: PMC3358320.

97. Rosenbluth RE, Cuddeford C, Baillie DL. Mutagenesis in Caenorhabditis elegans. II. A spectrum of mutational events induced with 1500 r of gamma-radiation. Genetics. 1985;109(3):493–511. Epub 1985/03/01. 3979812; PubMed Central PMCID: PMC1216284.

98. Zhang Y, Chen D, Smith MA, Zhang B, Pan X. Selection of reliable reference genes in Caenorhabditis elegans for analysis of nanotoxicity. PLoS One. 2012;7(3):e31849. Epub 2012/03/23. doi: 10.1371/journal.pone.0031849 22438870; PubMed Central PMCID: PMC3305280.

99. Friedman DB, Johnson TE. Three mutants that extend both mean and maximum life span of the nematode, Caenorhabditis elegans, define the age-1 gene. J Gerontol. 1988;43(4):B102–9. Epub 1988/07/01. doi: 10.1093/geronj/43.4.b102 3385139.

100. Sutphin GL, Kaeberlein M. Dietary restriction by bacterial deprivation increases life span in wild-derived nematodes. Exp Gerontol. 2008;43(3):130–5. Epub 2007/12/18. doi: 10.1016/j.exger.2007.10.019 18083317.


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